OPEN Coincidence of euxinia and impoverishment of in the aftermath of the - Famennian biotic crisis Krzysztof Broda1*, Leszek Marynowski2, Michał Rakociński1 & Michał Zatoń1

The lowermost Famennian deposits of the Kowala quarry (Holy Cross Mountains, ) are becoming famous for their rich content such as their abundant phosphatized remains (mostly thylacocephalans). Here, for the frst time, palaeontological and geochemical were integrated to document abundance and diversity patterns in the context of palaeoenvironmental changes. During deposition, the generally oxic to suboxic conditions were interrupted at least twice by the onset of photic zone euxinia (PZE). Previously, PZE was considered as essential in preserving phosphatised from, e.g., the famous Gogo Formation, . Here, we show, however, that during PZE, the abundance of arthropods drastically dropped. The phosphorous content during PZE was also very low in comparison to that from oxic-suboxic intervals where arthropods are the most abundant. As phosphorous is essential for phosphatisation but also tends to fux of the during bottom water , we propose that the PZE in such a case does not promote the fossilisation of the arthropods but instead to their impoverishment and non-preservation. Thus, the PZE conditions with anoxic bottom waters cannot be presumed as universal for exceptional fossil preservation by phosphatisation, and caution must be paid when interpreting the fossil abundance on the background of conditions.

1 Euxinic conditions in aquatic environments are defned as the presence of H2S and absence of . If such conditions occur at the in the water , where light is available, they are defned as photic zone euxinia (PZE). In these oxygen-free and hydrogen sulphide-rich environments, some (e.g., purple sul- phur bacteria or green sulphur bacteria) can thrive and photosynthesise, thereby playing a crucial role in the sulphur in stratifed basins2. In ancient sedimentary rocks, anoxygenic and thus the presence of PZE are best evidenced by the presence of specifc ‘molecular fossils’ (biomarkers), which are generated by anaerobic and photosynthetic bacteria3–5. PZE was an important environmental factor during the extinc- tion events in the ’s history, especially during oceanic anoxic events such as the end-Ordovician6, latest Devonian5 and end-Permian7. Te PZE has also been proposed as a factor leading to mass mortality events of fsh preserved in the Santana Formation8. Recently, researchers have emphasised that PZE played a crucial role in the exceptional preservation of phosphatic fossils in the famous Upper conservation deposits of the Gogo Formation in Australia2. In paper, we document the recurrent PZE conditions during sedimentation of the fossiliferous lower Famennian (Upper Devonian) deposits at the Kowala quarry (Holy Cross Mountains, Poland). Because of the great abundance and excellent preservation of phosphatic fossils of thylacocephalan, phyllocarid and angus- tidontid crustaceans9–12, articulated coelacanth fish13, conulariids14, coprolites15, as well as carbonaceous non-biomineralised algae16, these deposits were coined as the Kowala Lagerstätte9. Interestingly, these fossilif- erous deposits originated during the earliest Famennian, so in the afermath of the famous Frasnian-Famennian (F-F) biotic crisis, during which many marine groups sufered and, especially, col- lapsed17,18. Although intense volcanism has been considered as the most probable ultimate cause of the F-F event (e.g.19,20), the hypotheses concerning the exact proximate kill mechanism of the crisis difer21. However, the

1Department of Palaeontology and Stratigraphy, University of Silesia in Katowice, Faculty of Earth Sciences, Będzińska 60, 41-205, Sosnowiec, Poland. 2Department of Geochemistry, Mineralogy and Petrography, University of Silesia in Katowice, Faculty of Earth Sciences, Będzińska 60, 41-205, Sosnowiec, Poland. *email: [email protected]

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Figure 1. Locality of the studied section. (a) Location of the Kowala quarry on the background of the geology of the Holy Cross Mountains; (b) Te Kowala quarry with an exact position of the investigated section indicated (Google Maps, 2019).

common association of black “Kellwasser” facies near the F/F boundary22 supports the event might have been related to the transgression-related anoxia23,24. Combining palaeontology and geochemistry, we show that afer the F-F biotic crisis, the PZE still occurred intermittently during the early Famennian in the Late Devonian shelf basin of the southern margin of the Laurussia continent (present day Holy Cross Mountains, Poland). We also show that PZE did not to mass mortality events of arthropods, which abundantly inhabited the basin and, importantly, have not promoted their fossilisation as was considered previously. Our study shows that euxinic conditions should not be used as univer- sal explanation for exceptional fossil preservation. Instead, a strong caution must be paid when interpreting the taphonomy of phosphatised fossils and fuctuations of their abundance in the rock record. Geological Background Te active Kowala quarry is located in the southern limb of the Gałęzice-Bolechowice syncline in the southern part of the Kielce region of the Holy Cross Mountains (Fig. 1). During the Devonian, the Holy Cross Mountains area was part of a carbonate shelf that extended along the southern margin of the continent of Laurussia near the equator25–29. Te Famennian of the Kowala quarry were deposited in the intrashelf Chęciny-Zbrza basin28,30,31. Te lower Famennian deposits investigated in this paper are 21 m thick and crop out in a trench located in the north-central part of the quarry (N50°47′43,476′′, E20°33′53,568′′, Fig. 1). Te section comprises monotonous deposits of thin-bedded, dark, carbonaceous and thin-bedded, grey, micritic . Te investigated interval is confned to lithologic unit H-4 of Racki & Szulczewski32, which stratigraphically encom- passes the Late triangularis through Early marginifera conodont zones32. Earlier, the lower Famennian interval investigated in this paper was assumed as being confned to the crepida conodont Zone9,15, on the basis of lith- ological similarities and its position relative to the neighbouring trench section investigated by Marynowski et al.33. However, the new conodont dating showed that our section is slightly older and represents the Palmatolepis minuta minuta Zone (according to the latest conodont zonation of Spalletta et al.34), which corresponds to the previously established Late triangularis conodont Zone of Ziegler & Sandberg35. The conodont assemblage includes: Palmatolepis protorhomboidea, Pa. delicatula delicatula, Pa. superlobata, Polygnathus brevilaminus, Po. procerus, Icriodus alternatus alternatus, and Ic. deformatus deformatus. Te depositional environment is generally interpreted as deep shelf, below storm wave-base, but at least epi- sodically within the limits of the photic zone33,36–38. Material and Methods Collection of fossils. We collected 2029 specimens in total directly from the investigated section. At least 32 specimens were collected from each of the 34 investigated or marly shale beds, regardless of the preservation state or systematic position of the specimens. Te specimens were not retrieved from limestones as they are much harder to work with because they are very likely to be damaged while splitting the rock. For the purposes of this study, fossilised regurgitates, coprolites, and trace fossils were excluded, as they repre- sent the signs of activity, and not the animal itself. In some cases, the total abundance of some body fossils within each bed was difcult to establish because their tend to disarticulate post-mortem (crinoids, coelacanth fsh) or were extremely rare (angustidontid arthropods); these fossils were marked on diagrams but not evaluated quantitatively. Finally, we included 1840 of the 2029 specimens collected in situ in our quantitative palaeoecological analyses. Since during the feldwork, obtaining the same number of specimens for each bed was not always achievable and some of the collected specimens were excluded from the study, the general number of each fossil type in each bed was converted to a percentage contribution. Such a calculation allowed for comparisons with all the needed proportions being saved, despite the diferences in total number of specimens between the studied beds.

Total organic carbon (TOC) and total sulphur (TS) content. For total carbon (TC), total inorganic carbon (TIC) and total sulphur (TS) measurements, an ELTRA CS-500 IR-analyser was used (at Faculty of Earth Sciences, University of Silesia in Katowice, Poland). TOC was calculated as the diference between TC and TIC.

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Figure 2. Percentage contribution of the investigated lower Famennian body fossils from the Kowala quarry. Only specimens found in situ are included. Note that (linguloid + rhynchonellid) dominate the assemblage.

ELTRA standards were applied for the calibration. Values of better than ±2% for TC and ±3% for TIC were observed for analytical precision and accuracy (for more details see5).

Extraction, separation and derivatisation. An extraction of ground samples (<100 mesh) was per- formed using an accelerated Dionex ASE 350 solvent extractor by a mixture of dichloromethane (DCM)/metha- nol (1:1 v:v). For the extracts’ separation, micro-column (on Pasteur pipettes) chromatography was used. Silica gel was activated at 120 °C for 24 h, then cooled and poured into micro-columns. Extracts were separated into three fractions: aliphatic, aromatic, and polar, using: n-pentane, n-pentane and DCM (7:3 v:v), and DCM and metha- nol (1:1 v:v), respectively (for more details see39). For maleimide analysis, the polar fraction was again separated in micro-columns, using a DCM/acetone mixture (8:2 v:v). Ten, a DCM/acetone fraction was derivatised by MTBSTFA (N-tert-butyldimethylsilyl-N-methyltrifuoroacetamide). Samples were derivatised with MTBSTFA dissolved in super-dehydrated DCM, heated at 50 °C for 1 h, and analysed right afer derivatisation. Afer deriva- tisation, tert-butyl-dimethylsilyl derivatives of maleimides were obtained (see also40 and41).

Gas chromatography coupled with mass spectrometry (GC-MS). GC-MS analyses were carried out with an Agilent Technologies 7890 A gas chromatograph and Agilent 5975 C Network mass spectrometer with a Triple-Axis Detector (MSD). Separation was obtained on a fused silica capillary column (J&W HP5-MS, 60 m x 0.25 mm i.d., 0.25 µm flm thickness) coated with a chemically bonded phase (5% phenyl, 95% methylsiloxane). Te GC oven temperature was programmed from 45 °C (1 min) to 100 °C at 20 °C/min, and then to 300 °C at 3 °C/ min (hold 80 min), with a solvent delay of 10 min. Helium was used as a carrier gas at a constant fow of 2.6 ml/ min. Analyses were performed at the Faculty of Earth Sciences,, University of Silesia in Katowice, Poland. For more details see41.

Inorganic geochemistry. Te 34 pulp samples were analysed at Bureau Veritas Acme Labs Canada Ltd. Major, minor, and trace elements were analysed using inductively coupled plasma optical emission spectrometry (ICP-OES) and inductively coupled plasma mass spectrometry (ICP-MS) (details described in42). Te precision and accuracy of the results were better than ±0.05% (mostly ± 0.01%) for the major elements and generally better than ±1 ppm for the trace elements. Results Abundance and composition of fossil assemblages. In the studied assemblages (Figs 2 and 3), the most common fossils consisted of phosphatic shells of linguloid (Orbiculoidea sp.; 36.3%) and calcitic shells of rhynchonellid (25.4%) brachiopods. Interestingly, when Orbiculoidea brachiopods dominate, the relative abun- dance of rhynchonellids lowers and vice versa (Fig. 4). Te next most abundant assemblages are orthoconic nauti- loids (17.6%) preserved in the form of carbonaceous imprints of their or poorly preserved internal moulds. In general, they are more abundant in younger beds (Fig. 4). Te frst small peak in their percentage con- tribution occurs in beds Kow75 and Kow77 (12.5% and 13.33% respectively). Te next peak in relative abundance

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Figure 3. Examples of fossils from the investigated lower Famennian interval. Arthropods: (a) of thylacocephalan Concavicaris sp. af. bradleyi (GIUS 4-3622/T154a), (b) Pleon and of phyllocarid Echinocaris bisulcata Broda et al. 2019 (GIUS 4-3622/120-6), (c) Fragment of maxillipede of Angustidontus sp. (GIUS 4-3622/Kor110). Other fossils: (d) Shell of inarticulate Orbiculoidea sp. (GIUS 4-3622/ Kow190B/3 C), (e) Carbonaceous imprint of non-calcifying alga covered by numerous microconchid tubeworms (GIUS 4-3622/Kow190A/12), (f) Clustered bones and scales of a coelacanth fsh (GIUS 4-3654/21).

occurs in beds Kow106-Kow110 (max 20.69%). From bed Kow136 on, remains are present in every investigated bed. From that point on, their overall abundance gradually rises (with some minor fuctuations). In the lower part of bed Kow190 (Kow190A), their percentage contribution reaches the highest value of 63.46%. Tis and Kow160 are the only beds where are the most abundant component of the assemblage. Arthropods preserved as phosphatised are the third most abundant group. Concavicarid thylaco- cephalans (12.1%) and unidentifed (due to fragmentation and/or preservation state) arthropod remains (most probably Concavicarididae as well; 2.8%) are the most common arthropods. Te rarest arthropods of these units are phyllocarids with only 13 fossils (0.7%) found in situ and one single Angustidontidae (maxillipedes). Non-calcifying algae (1.8%), preserved as carbonaceous compressions, the bivalve Guerichia sp. (1.7%), cri- noid ossicles (1.0%), and coelacanth fsh bone clusters or isolated elements (0.5%), are all very rare (Figs 2 and 4). Tus, they have not been included in quantitative analyses.

Changes in arthropod abundance within the assemblages. In general, the percentage contribution of arthropod fossils decreases towards the younger beds (Fig. 4). Te most abundant arthropods are representa- tives of the Concavicarididae (Tylacocephala), whose abundance is characterised by several rapid changes with maximally 8%. Unidentifed arthropod remains (the majority represent Tylacocephala, as well) follow the same pattern as Tylacocephala fossils, with their maxima in the same beds (Fig. 4 and Table 3). In the case of

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Figure 4. Spindle diagrams showing the relative abundances of the main fossil groups from each investigated bed. On the same right side, the occurrences of Coelacanthiformes (1), Crinoidea (2), and Angustidontidae (3) are indicated. Euxinic levels are shaded. See Fig. 2 for an explanation of the symbols.

Phyllocarida, their relative abundance rises only in four intervals. In the intervals between these beds, no phyllo- carid remains were found (Fig. 4 and Table 1). Tese changes are also refected in the total number of the collected arthropod specimens (Fig. 5). Te number of specimens found in situ ranges from 0 (beds Kow 64, Kow 140) to 24 (bed Kow 72) and, in general, it grad- ually lowers towards the younger beds with tendency to difer between neighboring beds (Fig. 5). However, in some cases, when total number of acquired specimens lowers in the same beds, the percentage contribution of arthropods rises (Fig. 5). Specimen numbers per sample range between 9 (bed Kow 128) and 123 (bed Kow 188).

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Bed Tylacocephala Unid. Arthropoda Total Kow 190B 6.02 2.41 0 8.43 Kow 190A 6.73 0.96 0 7.69 Kow 188 0 1.63 0 1.63 Kow 182 4.35 0 0 4.35 Kow 180 12.12 0 0 12.12 Kow 178 1.09 0 1.09 2.18 Kow 172 24.44 11.11 0 35.55 Kow 170 11.86 3.39 0 15.25 Kow 168 8.62 0 0 8.62 Kow 160 1.61 0 0 1.61 Kow 156 13.21 5.66 0 18.87 Kow 154 1.89 1.89 0 3.78 Kow 152 4.08 0 0 4.08 Kow 150 16 0 2 18 Kow 148 9.09 9.09 5.46 23.64 Kow 146 16.49 4.12 2.06 22.67 Kow 142 16.67 10 13.33 40 Kow 140 0 0 0 0 Kow 136 0 0 1 1 Kow 128 33.33 0 0 33.33 Kow 114 68.18 18.18 0 86.36 Kow 110 33.33 2.56 0 35.89 Kow 108 16.67 6.67 0 23.34 Kow 106 3.45 0 0 3.45 Kow 86 5 0 0 5 Kow 84 8.82 5.88 0 14.7 Kow 82 8 12 4 24 Kow 78 33.33 0 0 33.33 Kow 76 6.25 2.08 0 8.33 Kow 72 31.94 1.39 0 33.33 Kow 70 33.33 7.69 0 41.02 Kow 68 24.19 4.84 0 29.03 Kow 66 24.53 7.55 0 32.08 Kow 64 0 0 0 0

Table 1. Relative abundances of arthropod groups (Tylacocephala, unidentifed arthropod remains and Phyllocarida) in each of the investigated beds. Te grey colour indicates the maximum percentage contribution of arthropods in comparison to the background values.

Generally, the fossil abundance rises towards the younger beds. However, three peaks of increased abundance (compared to the overall trend) were found: beds Kow 66–77, Kow 128–152 and Kow 172–190 b. In the lower part of the section (Kow 64–77), the changes in arthropod and total specimen numbers are simultaneous and similar in their amplitudes (the relative abundance does not change much). Tis applies also to the frst rise in fossil abundance (Kow 106–114). Te frst part of the second major peak of abundance (Kow 128–142) is, however, characterised by a drop in arthropod abundance. In bed Kow 140, we found no arthropod remains. Ten, in the second part of this peak (Kow 142–152), their abundance rises following the general trend, but with a much lower amplitude. In the last major peak, the number of arthropod specimens again drops gradually, with some minor peaks in beds Kow 172 (beginning of the total peak), Kow 180 and Kow 190; these changes, however, follow the opposite trend, i.e. the arthropod number rises while at decreasing sample size.

Organic geochemical data. Te results are presented in Table 2 and Fig. 6. Total organic carbon values are in a rather narrow range from 1.2% wt. to 4.6% wt. in our samples. In general, samples that are rich in carbonate are slightly depleted in organic carbon, but diferences in TOC content between and shales are minor. Te section is characterised by a low total sulphur concentration between 0% and 0.5% wt., but in most of the samples, it is below 0.1% wt. Steranes to hopanes ratio values are in the range of 0.5 to 0.8 (Table 2) which is similar to other parts of the Kowala section, including Annulata and Dasberg42,43, and lower than values noted for the Hangenberg secion5. Tese data imply that both algae and bacteria were important organisms contributing to the kerogen formation. Gammacerane, an indicator of water column stratifcation, was found in the all samples with relative concentra- tion also compatible to the other sections from the Kowala quarry42,43. Despite the small diferences in the TOC

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Aryl isoprenoids 2,3,6 diaryl Isorenieratane Ster/17α- Me,i-Bu/Me,Et Sample sum µg/gTOC isopren. µg/gTOC µg/g TOC hop G/H x1000 K190 11.24 2.15 1.83 0.75 0.04 1.68 K186 3.08 0.61 0.68 0.69 0.02 3.45 K183L 3.93 0.97 1.05 0.63 0.04 2.25 K182 3.26 6.08 5.21 0.64 0.03 2.42 K176 18.13 5.90 5.39 0.61 0.05 2.63 K170 2.74 1.09 1.14 0.62 0.03 2.76 K167L 2.94 2.57 2.09 0.61 0.04 0.00 K164 3.77 2.53 2.90 0.75 0.04 0.00 K162 9.93 5.36 5.69 0.73 0.07 2.96 K161L 6.64 4.36 4.85 0.67 0.07 1.03 K158 3.47 9.28 10.01 0.78 0.06 1.98 K151L 5.70 1.08 1.27 0.61 0.03 2.11 K150 4.87 1.06 1.13 0.76 0.03 2.46 K144 3.08 1.71 1.81 0.60 0.02 3.25 K143L 7.81 2.43 2.97 0.57 0.03 1.15 K138 4.36 1.17 1.32 0.72 0.03 2.38 K132 6.33 1.15 1.32 0.52 0.01 1.83 K124 8.40 2.24 2.32 0.63 0.03 3.01 K116 14.11 4.26 4.72 0.68 0.03 2.44 K115L 7.43 1.16 1.36 0.59 0.04 1.60 K112 8.10 3.89 5.22 0.59 0.04 2.31 K108 5.84 4.47 7.13 0.73 0.04 4.85 K107L 0.95 1.37 1.80 0.56 0.06 0.00 K103L 2.20 5.07 7.13 0.59 0.06 0.00 K102 10.75 4.15 6.46 0.61 0.05 2.53 K101L 30.00 10.09 26.02 0.72 0.09 0.90 K100 7.95 3.12 5.50 0.69 0.08 3.37 K98 5.41 3.08 2.55 0.60 0.08 3.85 K90 7.58 0.49 0.36 0.56 0.04 3.90 K82 3.14 1.07 1.17 0.54 0.06 2.80 K75L 12.73 7.51 6.29 0.49 0.13 1.05 K74 3.42 0.49 0.55 0.51 0.06 2.98 K71L 3.24 0.35 0.33 0.49 0.07 1.97 K64 3.14 0.42 0.44 0.48 0.07 3.34

Table 2. Aryl isoprenoids, isorenieratane and palaeorenieratane concentrations, steranes and hopanes ratios and the 2-methyl-3-iso-butyl- to 2-methyl-3-ethyl-maleimide ratio. Ster/17α-hop = steranes consist of the C27, C28, C29 ααα(20 S + 20 R), αββ(20 S + 20 R) and diasteranes, 17α-hopanes consist of the C27 to C35 pseudohomologues (with 22 S and 22 R epimers). G/H = Gammacerane/C30 17α-hopane ratio.

content, important changes in isorenieratane concentrations were found (Fig. 6). Tis compound is a biomarker of green sulphur bacteria and acts as an indicator of euxinic conditions in the photic zone of the water column3,38. Two maxima in isorenieratane concentrations were identifed (Table 2 and Fig. 6). Te frst is in the lower part of the section (around bed Kow 100), reaching 25 µg/g TOC and the second, smaller maximum (±10 µg/g TOC) in the upper part of the section. Moreover, isorenieratane closely correlates with the 2,3,6−/3,4,5-diaryl isoprenoid, i.e., the so called palaeorenieratane (R2 = 0.95), which usually co-occurs with isorenieratane in Palaeozoic sedi- mentary rocks (e.g.4,42–49). Additionally, there is a strong correlation with the concentration of aryl isoprenoids, which are compounds that are degradation products of isorenieratane (e.g.3,48,50) (R2 = 0.7). In almost all samples the maleimides (1H-pyrrole-2,5-diones), decomposition products of chlorophylls and bacteriochlorophylls, were identifed as the abundant group of compounds from the polar fraction. Between maleimides, those treated as of bacteriochlorophyll origin (with 2-methyl-3-iso-butyl- confguration; Me,i-Bu) were present in almost all samples. However, the Me,i-Bu to Me,Et (2-methyl-3-ethyl-) maleimide ratio40,51,52 does not correlate with the isorenieratane and palaeorenieratane concentrations.

Inorganic geochemical data. Te T/U ratio in almost all carbonate-rich/ samples is >1, which is indicative of oxic conditions. Only three samples from the lower part of the investigated section reached T/U ratio values below 1, which imply dysoxic bottom water conditions. Te lower values of the T/U ratio in shales (<3) are indicative of oxygen depleted conditions in the whole analysed section (Fig. 6). Te V/Cr ratios range from 1.21 to 9.03 (Table 3); these values are indicative of oxic through dysoxic to anoxic conditions (e.g.5,53). Te V/Cr ratio shows a good correlation with Mo as well as the isorenieratane contents. Additionally, the Corg/P ratio

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Figure 5. Changes in the abundance of body fossils in the investigated section. Abbreviations: 1, total number of body fossils; 2, number of arthropod fossils (Tylacocephala + Phyllocarida + unidentifed arthropod remains). Te euxinic levels are shaded. Te amount of phosphorous in particular samples is marked with a red line.

also closely corresponds with these data (Fig. 6 and Table 3). Te maximum values of the Corg/P ratio around bed Kow 101 (frst postulated anoxic interval) reached from 116.92 to 212.47, while in the second anoxic interval located between Kow 158 and Kow 162, the ratios reached values from 193.16 to 768.5 Corg/P, respectively. All results are presented in Table 3 and in Fig. 6.

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TOC TS P U T V Cr Mo Sample [%] [%] (%) (ppm) (ppm) (ppm) (ppm) (ppm) T/U V/Cr Corg/P Kow190A 3.54 0.05 0.06 3.4 6.9 195 61.58 2.2 2.03 3.17 57.96 Kow 186 3.65 0.15 0.13 2.5 7 96 61.58 0.8 2.80 1.56 27.86 Kow 183 2.11 0.03 0.07 1.2 2.2 36 20.53 1.1 1.83 1.75 28.46 Kow 182 3.39 0.02 0.03 2.6 6.2 119 54.74 0.6 2.38 2.17 129.36 Kow 176 1.56 0.06 0.04 2.7 5.5 115 47.89 0.4 2.04 2.40 39.80 Kow 170 4.63 0.03 0.10 2.7 5.7 84 54.74 0.5 2.11 1.53 48.27 Kow 167 0.63 0.12 0.05 1.1 1.9 33 27.37 0.2 1.73 1.21 13.07 Kow 164 1.91 0.38 0.07 3.3 6.4 157 61.58 0.8 1.94 2.55 29.13 Kow 162 3.55 0.01 0.02 3.3 6.1 249 54.74 2.3 1.85 4.55 203.12 Kow 161 3.35 0.05 0.00 1.5 2.2 90 20.53 2.4 1.47 4.38 768.50 Kow 158 3.37 0.02 0.02 3.3 5.7 225 41.05 2.3 1.73 5.48 193.16 Kow 151 2.15 0.01 0.02 1.7 3.7 60 34.21 0.4 2.18 1.75 123.45 Kow 150 3.83 0.03 0.07 3.3 6.2 117 54.74 0.7 1.88 2.14 51.62 Kow 144 3.62 0.04 0.08 2.7 5.8 113 54.74 0.9 2.15 2.06 46.08 Kow 143 1.27 0.01 0.01 1.1 2 46 13.68 0.3 1.82 3.36 97.03 Kow 138 3.18 0.01 0.07 2.9 6.8 121 54.74 0.3 2.34 2.21 42.88 Kow 132 2.06 0.09 0.09 1.6 3.9 62 34.21 0.7 2.44 1.81 23.58 Kow 124 2.93 0.04 0.06 3.2 5.5 108 54.74 0.4 1.72 1.97 47.89 Kow 116 1.20 0.00 0.10 2.6 6 100 54.74 0.4 2.31 1.83 11.97 Kow 115 2.84 0.00 0.02 1.2 1.8 43 20.53 0.5 1.50 2.09 130.20 Kow 112 3.61 0.01 0.02 2.7 4.3 156 47.89 0.7 1.59 3.26 165.57 Kow 108 2.32 0.39 0.03 2.7 5.9 260 61.58 1.4 2.19 4.22 88.41 Kow 107 0.48 0.32 0.01 0.6 1 47 20.53 3.1 1.67 2.29 36.47 Kow 103 0.73 0.09 0.01 0.8 1.3 57 20.53 0.8 1.63 2.78 55.80 Kow 102 4.64 0.03 0.02 2.9 5.7 200 47.89 1.3 1.97 4.18 212.47 Kow 101 2.50 0.08 0.01 1.4 1.1 27 6.84 3.2 0.79 3.95 191.09 Kow 100 3.57 0.39 0.03 3.2 6 156 47.89 2.7 1.88 3.26 116.92 Kow 98 1.62 0.36 0.04 2.8 6.2 142 54.74 1.7 2.21 2.59 41.34 Kow 90 2.31 0.52 0.16 3.7 8.1 90 61.58 0.4 2.19 1.46 14.71 Kow 82 3.65 0.01 0.08 11.5 5.7 162 47.89 0.3 0.50 3.38 43.97 Kow 75 1.76 0.00 0.02 4.2 3.4 247 27.37 2.1 0.81 9.03 100.87 Kow 74 4.36 0.02 0.09 11.2 4.5 115 41.05 0.3 0.40 2.80 47.56 Kow 71 4.47 0.02 0.06 1.8 1.7 52 13.68 0.4 0.94 3.80 78.75 Kow 64 3.02 0.00 0.13 8.5 4.5 142 47.89 0.3 0.53 2.96 23.06

Table 3. Geochemical data of the samples from the lower Famennian Kowala section: TOC, TS, P, U, T, V, Cr, Mo content and values of the T/U, V/Cr and Corg/P ratios. Limestones are marked in grey.

Discussion Changes of sedimentary conditions. Despite the monotonous lithology, similar TOC content through the entire section and only minor fuctuations between the algae and bacteria as a kerogen contributors (see ster- anes to hopanes ratio in Table 2), organic and inorganic proxies indicate signifcant changes in depositional con- ditions and abundance of some fossil groups. Tere are two visible spikes of isorenieratane, palaeorenieratane and aryl isoprenoid concentrations (Fig. 6; Table 1). Te frst is located in the lowermost part of the section, around sample Kow 101, and the second is in the upper part, between samples Kow 158 and Kow 162 (Fig. 6). Similar patterns were observed for the Mo concentration and V/Cr ratio, which reached their maxima at the same strati- graphic levels (Fig. 6). Te third, smaller isorenieratane spike that correlated with higher concentrations of Mo, V/ Cr and Corg/P ratios is observable in the lowermost part of the section in sample Kow 75 (Fig. 6). Conversely, inor- ganic proxies based on the uranium (T/U and Uautig) and maleimide ratios are not in agreement with the above parameters. Te discrepancy between the U proxies and Mo concentration and the V/Cr ratio in the upper part of the section is unclear, especially since all these parameters work closely together in the other Upper Devonian sections from the Kowala quarry, such as those containing the Annulata or Hangenberg events5,42. Notably, part of the uranium was transported to the basin with a detrital fraction, which, in consequence, changed the ratio between the detrital T and U connected with primary . However, the lack of correlation between U and Al (R2 = 0.11) does not confrm this mechanism as a reliable factor. Te other, more likely explanation of disagreement between T/U and the other proxies is based on the assumption, that the euxinic zone was located in the water column but did not reach, or only periodically reached, the sea-foor (as it was shown in43). Uranium was partially diluted from the sediment afer deposition during oxic periods, while Mo connected with framboids54 formed in the water column and survived intermittent oxygenation on the seafoor. Particulate

Scientific Reports | (2019)9:16996 | https://doi.org/10.1038/s41598-019-52784-4 9 www.nature.com/scientificreports/ www.nature.com/scientificreports ) Total — TOC [%], ( b ) Total content carbon organic ( a ) Total data. proxy biomarker and inorganic as well as carbon, organic section showing Famennian the lower of plot Composite Figure 6 . Figure ratio, total to carbon organic f ) Total ( ratio, chromium to ( e ) Te ratio, uranium to thorium ( d ) Te [ppm], content molybdenum [%], ( c ) Total content phosphorus mudstones. indicate while arrows black limestones ( μ g/g TOC). Red arrowsindicate concentration ( g ) Isorenieratane

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shuttle cannot be excluded as a process driving Mo concentration, but this element does not correspond to the correlation between inorganic and organic indicators. Te lack of correlation between the isorenieratane concentration and the Me,i-Bu to Me,Et maleimide ratio is much easier to explain. Te origin of Me,i-Bu-maleimides is connected with green sulphur bacteria while Me,Et-maleimides are degradation products of both chlorophyll and bacteriochlorophyll40,51. Tis implies that Me,i-Bu to Me,Et maleimide ratio values are not only dependent on green sulphur bacteria (GSB) blooms but also on the fowering of algae and other that generate chlorophyll. Tus, Me,i-Bu-maleimides are useful indicators of GSB occurrence, but the Me,i-Bu to Me,Et maleimide ratio does not necessarily illustrate the intensity of euxinia. Gammacerane, an indicator of water column stratifcation55 was found in the all investigated samples and the values of G/H ratio are quite stable across the section (Table 2). Tis implies, that anaerobic , which are precursors of gammacerane55, were constantly present in water column and most possibly fed on green sulphur bacteria. Te presence of gammacerane also indicates a permanent stratifcation of water column in the afermath of F/F crisis. Te next proxy that is in accordance with the other proxies used here is the Corg/P ratio. Te values of the Corg/P ratio, ranging from 30 to 150, are characteristic for high productivity and periodically oxygen-restricted 56 conditions (see ), while the higher values of the Corg/P ratio (>150) are indicative for high-productivity and permanent anoxic conditions on the seafoor. In the case of the investigated section, higher values of Corg/P are in agreement with the Mo, V/Cr and isorenieratane values, thus confrming a higher productivity and seafoor euxinia (Fig. 6). Based on isorenieratane, palaeorenieratane and aryl isoprenoid concentrations, as well as the Mo concen- tration, V/Cr and Corg/P ratio values, the following scenario of depositional conditions during the triangularis zone of the early Famennian can be presented. At the frst stage of deposition, conditions were dysoxic to anoxic on the seafoor with photic zone euxinia (PZE) reaching (periodically?) the bottom waters. Ten, the conditions became more aerobic, which took place between sedimentation of the layers K112 and K151. Te second event saw anoxia/euxinia occurring between the formation of the layers K158 and K167. During sedimentation of the uppermost part of the section, oxygenation of the bottom waters prevailed again, while the water column above may have still witnessed some PZE. Te episodes with domination of euxinia in the bottom part of the water column are shaded on Fig. 6.

Relationship between redox changes and fossil abundance. Depositional conditions are an important factor controlling the state of fossil preservation57, and, euxinia/anoxia/dysoxia and water col- umn stratifcation played an important role in the exceptional preservation of past organisms2,58. At Kowala, the lower Famennian section investigated here is regarded as an example of a conservation deposit, possess- ing well-preserved, abundant and diverse assemblages of arthropods, fsh and non‐biomineralised macroal- gae9,13,16, even with sporadic cases of sof tissue preservation59. Interestingly, this fossiliferous interval falls within the lowermost Famennian triangularis Zone that marks the immediate afermath of the Frasnian-Famennian biotic crisis. During this time interval, oxygen-defcient conditions in the Kowala basin occurred as confrmed through -ray spectrometry60, as well as geochemical and petrographic studies43. Terefore, taking these fndings into account, we have expected that the highest number of exceptionally preserved fossils (especially phosphatised arthropods) occur in horizons characterised by elevated anoxia/euxinia, especially since the PZE has been considered as an important factor in preserving fossils in Upper Devonian Lagerstätte deposits such as the Australian Gogo Formation2. However, we found increased amounts of thylacocephalan arthropods at intervals where conditions were rather suboxic and PZE did not reach the seafoor (Figs 4, 5). Tese intervals of higher abundance of arthropods especially embrace the section from samples K112 to K128, K142 to K150, and K171 to K175 (non-shaded parts of the section in Figs 4 and 5). In the case of other fossils having originally phosphatic shells such as orbiculoid brachiopods, which are the most abundant fossils occurring throughout the studied section (Fig. 4), such ten- dencies were not observed. It is possible that these organisms could have colonised the sea-bottom only during short oxygenated pulses in the otherwise suboxic bottom waters (e.g.5,61,62,). However, considering their large abundance throughout the studied section, irrespective of the anoxic events, it is even more probable that the orbiculoids were epiplanktonic63; these orbiculoids would have drifed in the surface waters attached to algae occurring in the same deposits16, or would have functioned as opportunistic bottom dwellers able to thrive in stressed, oxygen-defcient conditions as other linguloid brachiopods known from the Devonian64. Our data show that arthropods (and especially dominant thylacocephalans) were common only during oxic/ suboxic periods (Figs 5, 6) with a thin PZE located in the water column above43, while more restricted conditions were unfavourable for this group of organisms. Te mode of of thylacocephalans is still problematic. Tey have been interpreted either as nektonic pred- ators65, benthic ambush predators, or benthic scavengers66–68. For some species (mostly protozoeids), nektonic mode of life was proposed on the basis of such features as their small size, elongated carapace and hyperthrophied eyes69,70. A nektobenthic mode of life of thylacocephalans instead, has been proposed by various authors (e.g.67,71) based on such features as reduced posterior trunk , lack of a fexible (see11,70,72) and their rather thin, poorly mineralised cuticles68,73. However the last feature is shared with some nektonic arthropods, like amphipods74, so except the last one, these features can be observed in modern nektobenthic (both swimming and seafoor-dwelling75). Although the of both raptorial and posterior appendages of the Kowala thylacocephalans remains unknown, the anatomy and architecture of their carapaces were described by Broda and Zatoń10. Te authors pointed out an additional important feature: the presence of “sensory belts” in the upper and lower margins of the carapace. Te authors assumed that these zones, consisting of many organule canals, are the remnants of a highly developed sensory system that can monitor the surrounding space. Such a

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developed set of sensors could allow these predators to easily fnd their prey either in the surrounding water col- umn, or hiding on the sea bottom. Such sensors could have also served as anti-predatory “alarm device”. However, taking all these known features into account, we are still not sure about the exact thylacocephalan mode of life. Depending on species, it would probably be either nektonic or necto-benthic organism. Te lack of arthropod fossils in euxinic intervals (Figs 3 and 5), however doesn’t have to be necessarily con- nected with unfavourable living conditions. Based on modern examples from the Santa Monica Basin, the , the Baltic Sea and other basins, anoxic conditions at the seafoor promote phosphorous fux out of the sed- iment76–78. Tis is in accordance with P concentrations throughout the section, showing its lowermost values exactly within the euxinic levels (Fig. 6). At the same levels, Corg/P ratio values are also the highest. As shown by Zatoń et al.9, exoskeletal remains of all arthropods from the Late Devonian of the Kowala quarry are phosphatic. Apparently, a lack of sufcient phosphorous in sediments during the euxinic periods precluded arthropod pres- ervation and in consequence controlled the overall fossilisation processes of the arthropod . Te abundance of arthropod exoskeletons in rocks characterised by suboxic conditions during their sedimentation coincides with much higher values of P (Figs 4 and 5). Phosphatisation requires a special microenvironment characterised by a specifc pH, redox conditions and a sufcient concentration of P79–82. Tus, all parameters pro- moting phosphatisation of the arthropod appear to have been present in the Kowala suboxic environment. Te alternative hypothesis, which assumes mass mortality events that may have occurred during euxinic events (e.g.8), is not supported in our case. Tis is primarily because the PZE intervals in the studied section are depleted in fossil arthropods. In conclusion, the post-Frasnian-Famennian crisis interval in the Kowala quarry is rich in the opportunistic benthic linguloid brachiopod Orbiculoidea, orthoconic nautiloids and phosphatised remains of arthropods, among which Tylacocephala dominate. As linguloid brachiopods occur throughout the studied section, the arthropods appear to be absent in intervals when PZE was detected. Te simultaneous drop in phosphorous content in the euxinic intervals indicates that the absence of arthropods resulted rather from their non-preservation due to low P content than from changes in palaeoenvironmental conditions. Tus, in this case, euxinic/anoxic conditions negatively infuenced the preservation of arthropod via phosphati- sation instead of promoting their fossilisation as has been suggested in an earlier study2. Apparently, PZE con- ditions were not universal for fossil preservation through phosphatisation. Tus, any interpretations concerning the abundance of fossils within euxinic horizons should be treated with caution, and taphonomic causes may be crucial, primary factors in controlling the presence or absence of fossils in the rock record.

Received: 25 July 2019; Accepted: 18 October 2019; Published: xx xx xxxx

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Prof. Katarzyna Narkiewicz (National Geological Institute) is thanked for dating the section using conodonts, which was fnancially supported by the MAESTRO grant No. 2013/08/A/ST10/00717 (for Grzegorz Racki). Te rest of the study was fnanced by the PRELUDIUM grant 2015/19/N/ST10/01527 (for Krzysztof Broda). Christian Klug, an anonymous reviewer and the Editor Luis A. Buatois are acknowledged for their useful remarks and constructive comments which helped to improve the fnal version of the manuscript. Author contributions K.B., feldworks, sample preparation, fossil data analyses, preparation of fgures; L.M., organic geochemistry analyses and results interpretation; M.R., inorganic geochemistry analyses and results interpretation; M.Z., data analyses, interpretations and supervision over the text. All authors participated in manuscript preparation. Competing interests Te authors declare no competing interests. Additional information Correspondence and requests for materials should be addressed to K.B. Reprints and permissions information is available at www.nature.com/reprints. Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional afliations. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Cre- ative Commons license, and indicate if changes were made. Te images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not per- mitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

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